Whole-genome discovery of miRNAs and their targets in wheat (Triticum aestivum L.)

BMC Plant Biology

Volumn 14, Issue 1, 2014, Pages

  Sun, Fenglong ^a   Guo, Guanghui ^a   Du, Jinkun ^a   Guo, Weiwei ^a   Peng, Huiru ^a   Ni, Zhongfu ^a   Sun, Qixin ^a   Yao, Yingyin ^a  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; MICRORNA; NUCLEOTIDE; TRANSCRIPTOME;

ANTIBODY SPECIFICITY; GENE EXPRESSION REGULATION; GENE LIBRARY; GENETICS; GROWTH, DEVELOPMENT AND AGING; HORDEUM; METABOLISM; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; PLANT GENOME; REPRODUCIBILITY; RNA STABILITY; SPECIES DIFFERENCE; WHEAT;

BLOTTING, NORTHERN; CONSERVED SEQUENCE; DNA, COMPLEMENTARY; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; GENE LIBRARY; GENOME, PLANT; HORDEUM; MICRORNAS; NUCLEOTIDES; ORGAN SPECIFICITY; REPRODUCIBILITY OF RESULTS; RNA STABILITY; SPECIES SPECIFICITY; TRANSCRIPTOME; TRITICUM;

EID: 84902104114     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/1471-2229-14-142     Document Type: Article

References (71)

1. Voinnet O. Origin, biogenesis, and activity of plant microRNAs. Cell 2009, 136(4):669-687. 10.1016/j.cell.2009.01.046, 19239888.
2. Bartel D. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004, 116:281-297. 10.1016/S0092-8674(04)00045-5, 14744438.
3. Jones-Rhoades MW, Bartel DP, Bartel B. MicroRNAs and their regulatory roles in plants. Annu Rev Plant Biol 2006, 57:19-53. 10.1146/annurev.arplant.57.032905.105218, 16669754.
4. Lee Y, Ahn C, Han J, Choi H, Kim J, Yim J, Lee J, Provost P, Radmark O, Kim S, Kim VN. The nuclear RNase III Drosha initiates microRNA processing. Nature 2003, 425(6956):415-419. 10.1038/nature01957, 14508493.
5. Park W, Li J, Song R, Messing J, Chen X. Carpel factory, a dicer homolog, and HEN1, a novel protein, act in micro-RNA metabolism in Arabidopsis thaliana. Curr Biol 2002, 12:1484-1495. 10.1016/S0960-9822(02)01017-5, 12225663.
6. Yu B, Wang H. Translational inhibition by microRNAs in plants. Prog Mol Subcell Biol 2010, 50:41-57. 10.1007/978-3-642-03103-8_3, 19841880.
7. Chen X. Small RNAs and their roles in plant development. Annu Rev Cell Dev Biol 2009, 25:21-44. 10.1146/annurev.cellbio.042308.113417, 19575669.
8. Mallory AC, Vaucheret H. Functions of microRNAs and related small RNAs in plants. Nat Genet 2006, 38(Suppl):S31-S36.
9. Kozomara A, Griffiths-Jones S. miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res 2014, 42(Database issue):D68-D73. 3965103, 24275495.
10. Kutter C, Schob H, Stadler M, Meins F, Si-Ammour A. MicroRNA-mediated regulation of stomatal development in Arabidopsis. The Plant cell 2007, 19(8):2417-2429. 10.1105/tpc.107.050377, 2002609, 17704216.
11. Pang M, Woodward AW, Agarwal V, Guan X, Ha M, Ramachandran V, Chen X, Triplett BA, Stelly DM, Chen ZJ. Genome-wide analysis reveals rapid and dynamic changes in miRNA and siRNA sequence and expression during ovule and fiber development in allotetraploid cotton (Gossypium hirsutum L.). Genome Biol 2009, 10(11):R122. 10.1186/gb-2009-10-11-r122, 3091316, 19889219.
12. Zhu QH, Spriggs A, Matthew L, Fan L, Kennedy G, Gubler F, Helliwell C. A diverse set of microRNAs and microRNA-like small RNAs in developing rice grains. Genome Res 2008, 18(9):1456-1465. 10.1101/gr.075572.107, 2527712, 18687877.
13. Zabala G, Campos E, Varala KK, Bloomfield S, Jones SI, Win H, Tuteja JH, Calla B, Clough SJ, Hudson M, Vodkin LO. Divergent patterns of endogenous small RNA populations from seed and vegetative tissues of Glycine max. BMC Plant Biol 2012, 12:177. 10.1186/1471-2229-12-177, 3534067, 23031057.
14. Ng DW, Zhang C, Miller M, Palmer G, Whiteley M, Tholl D, Chen ZJ. cis- and trans-Regulation of miR163 and target genes confers natural variation of secondary metabolites in two Arabidopsis species and their allopolyploids. Plant Cell 2011, 23(5):1729-1740. 10.1105/tpc.111.083915, 3123960, 21602291.
15. Niwa R, Slack FJ. The evolution of animal microRNA function. Current Opinion Gen Dev 2007, 17(2):145-150.
16. Ha M, Pang M, Agarwal V, Chen ZJ. Interspecies regulation of microRNAs and their targets. Biochim Biophys Acta 2008, 1779(11):735-742. 10.1016/j.bbagrm.2008.03.004, 2586835, 18407843.
17. Brodersen P, Sakvarelidze-Achard L, Bruun-Rasmussen M, Dunoyer P, Yamamoto YY, Sieburth L, Voinnet O. Widespread translational inhibition by plant miRNAs and siRNAs. Science 2008, 320(5880):1185-1190. 10.1126/science.1159151, 18483398.
18. Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel B, Bartel DP. Prediction of plant microRNA targets. Cell 2002, 110(4):513-520. 10.1016/S0092-8674(02)00863-2, 12202040.
19. Jones-Rhoades MW, Bartel DP. Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 2004, 14(6):787-799. 10.1016/j.molcel.2004.05.027, 15200956.
20. German MA, Pillay M, Jeong DH, Hetawal A, Luo S, Janardhanan P, Kannan V, Rymarquis LA, Nobuta K, German R, De Paoli E, Lu C, Schroth G, Meyers BC, Green PJ. Global identification of microRNA-target RNA pairs by parallel analysis of RNA ends. Nat Biotechnol 2008, 26(8):941-946. 10.1038/nbt1417, 18542052.
21. Addo-Quaye C, Eshoo TW, Bartel DP, Axtell MJ. Endogenous siRNA and miRNA targets identified by sequencing of the Arabidopsis degradome. Current Biol CB 2008, 18(10):758-762.
22. Li YF, Zheng Y, Addo-Quaye C, Zhang L, Saini A, Jagadeeswaran G, Axtell MJ, Zhang W, Sunkar R. Transcriptome-wide identification of microRNA targets in rice. Plant J 2010, 62(5):742-759. 10.1111/j.1365-313X.2010.04187.x, 20202174.
23. Shamimuzzaman M, Vodkin L. Identification of soybean seed developmental stage-specific and tissue-specific miRNA targets by degradome sequencing. BMC Genomics 2012, 13:310. 10.1186/1471-2164-13-310, 3410764, 22799740.
24. Tang Z, Zhang L, Xu C, Yuan S, Zhang F, Zheng Y, Zhao C. Uncovering small RNA-mediated responses to cold stress in a wheat thermosensitive genic male-sterile line by deep sequencing. Plant Physiol 2012, 159(2):721-738. 10.1104/pp.112.196048, 3375937, 22508932.
25. Montgomery TA, Yoo SJ, Fahlgren N, Gilbert SD, Howell MD, Sullivan CM, Alexander A, Nguyen G, Allen E, Ahn JH, Carrington JC. AGO1-miR173 complex initiates phased siRNA formation in plants. Proc Natl Acad Sci U S A 2008, 105(51):20055-20062. 10.1073/pnas.0810241105, 2598728, 19066226.
26. Cuperus JT, Carbonell A, Fahlgren N, Garcia-Ruiz H, Burke RT, Takeda A, Sullivan CM, Gilbert SD, Montgomery TA, Carrington JC. Unique functionality of 22-nt miRNAs in triggering RDR6-dependent siRNA biogenesis from target transcripts in Arabidopsis. Nat Struct Mol Biol 2010, 17(8):997-1003. 10.1038/nsmb.1866, 2916640, 20562854.
27. Chen HM, Chen LT, Patel K, Li YH, Baulcombe DC, Wu SH. 22-Nucleotide RNAs trigger secondary siRNA biogenesis in plants. Proc Natl Acad Sci U S A 2010, 107(34):15269-15274. 10.1073/pnas.1001738107, 2930544, 20643946.
28. Allen E, Xie Z, Gustafson AM, Carrington JC. microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 2005, 121(2):207-221. 10.1016/j.cell.2005.04.004, 15851028.
29. Wang Y, Itaya A, Zhong X, Wu Y, Zhang J, van der Knaap E, Olmstead R, Qi Y, Ding B. Function and evolution of a MicroRNA that regulates a Ca2 + -ATPase and triggers the formation of phased small interfering RNAs in tomato reproductive growth. Plant Cell 2011, 23(9):3185-3203. 10.1105/tpc.111.088013, 3203446, 21917547.
30. Kantar M, Lucas SJ, Budak H. miRNA expression patterns of Triticum dicoccoides in response to shock drought stress. Planta 2011, 233(3):471-484. 10.1007/s00425-010-1309-4, 21069383.
31. Meng F, Liu H, Wang K, Liu L, Wang S, Zhao Y, Yin J, Li Y. Development-associated microRNAs in grains of wheat (Triticum aestivum L.). BMC Plant Biol 2013, 13:140. 10.1186/1471-2229-13-140, 4015866, 24060047.
32. Yao Y, Guo G, Ni Z, Sunkar R, Du J, Zhu JK, Sun Q. Cloning and characterization of microRNAs from wheat (Triticum aestivum L.). Genome Biol 2007, 8(6):R96. 10.1186/gb-2007-8-6-r96, 2394755, 17543110.
33. Li Y-F, Zheng Y, Jagadeeswaran G, Sunkar R. Characterization of small RNAs and their target genes in wheat seedlings using sequencing-based approaches. Plant Sci 2013, 203-204:17-24.
34. Wang B, Sun YF, Song N, Wang XJ, Feng H, Huang LL, Kang ZS. Identification of UV-B-induced microRNAs in wheat. Genet Mol Res 2013, 12(4):4213-4221. 10.4238/2013.October.7.7, 24114216.
35. Wei B, Cai T, Zhang R, Li A, Huo N, Li S, Gu YQ, Vogel J, Jia J, Qi Y, Mao L. Novel microRNAs uncovered by deep sequencing of small RNA transcriptomes in bread wheat (Triticum aestivum L.) and Brachypodium distachyon (L.) Beauv. Funct Integr Genomics 2009, 9(4):499-511. 10.1007/s10142-009-0128-9, 19499258.
36. Xin M, Wang Y, Yao Y, Xie C, Peng H, Ni Z, Sun Q. Diverse set of microRNAs are responsive to powdery mildew infection and heat stress in wheat (Triticum aestivum L.). BMC Plant Biol 2010, 10:123. 10.1186/1471-2229-10-123, 3095282, 20573268.
37. Jin W, Li N, Zhang B, Wu F, Li W, Guo A, Deng Z. Identification and verification of microRNA in wheat (Triticum aestivum). J Plant Res 2008, 121(3):351-355. 10.1007/s10265-007-0139-3, 18357413.
38. Sunkar R, Jagadeeswaran G. In silico identification of conserved microRNAs in large number of diverse plant species. BMC Plant Biol 2008, 8:37. 10.1186/1471-2229-8-37, 2358906, 18416839.
39. Lucas SJ, Budak H. Sorting the wheat from the chaff: identifying miRNAs in genomic survey sequences of Triticum aestivum chromosome 1AL. PLoS One 2012, 7(7):e40859. 10.1371/journal.pone.0040859, 3398953, 22815845.
40. Brenchley R, Spannagl M, Pfeifer M, Barker GL, D'Amore R, Allen AM, McKenzie N, Kramer M, Kerhornou A, Bolser D, Kay S, Waite D, Trick M, Bancroft I, Gu Y, Huo N, Luo MC, Sehgal S, Gill B, Kianian S, Anderson O, Kersey P, Dvorak J, McCombie WR, Hall A, Mayer KF, Edwards KJ, Bevan MW, Hall N. Analysis of the bread wheat genome using whole-genome shotgun sequencing. Nature 2012, 491(7426):705-710. 10.1038/nature11650, 3510651, 23192148.
41. Ling HQ, Zhao S, Liu D, Wang J, Sun H, Zhang C, Fan H, Li D, Dong L, Tao Y, Gao C, Wu H, Li Y, Cui Y, Guo X, Zheng S, Wang B, Yu K, Liang Q, Yang W, Lou X, Chen J, Feng M, Jian J, Zhang X, Luo G, Jiang Y, Liu J, Wang Z, Sha Y, et al. Draft genome of the wheat A-genome progenitor Triticum urartu. Nature 2013, 496(7443):87-90. 10.1038/nature11997, 23535596.
42. Jia J, Zhao S, Kong X, Li Y, Zhao G, He W, Appels R, Pfeifer M, Tao Y, Zhang X, Jing R, Zhang C, Ma Y, Gao L, Gao C, Spannagl M, Mayer KF, Li D, Pan S, Zheng F, Hu Q, Xia X, Li J, Liang Q, Chen J, Wicker T, Gou C, Kuang H, He G, Luo Y, et al. Aegilops tauschii draft genome sequence reveals a gene repertoire for wheat adaptation. Nature 2013, 496(7443):91-95. 10.1038/nature12028, 23535592.
43. Tanaka T, Kobayashi F, Joshi GP, Onuki R, Sakai H, Kanamori H, Wu J, Simkova H, Nasuda S, Endo TR, Hayakawa K, Dolezel J, Ogihara Y, Itoh T, Matsumoto T, Handa H. Next-generation survey sequencing and the molecular organization of wheat chromosome 6B. DNA Res 2013,
44. Kurtoglu KY, Kantar M, Lucas SJ, Budak H. Unique and conserved microRNAs in wheat chromosome 5D revealed by next-generation sequencing. PLoS One 2013, 8(7):e69801. 10.1371/journal.pone.0069801, 3720673, 23936103.
45. Vensel WH, Tanaka CK, Cai N, Wong JH, Buchanan BB, Hurkman WJ. Developmental changes in the metabolic protein profiles of wheat endosperm. Proteomics 2005, 5(6):1594-1611. 10.1002/pmic.200401034, 15800972.
46. Wan Y, Poole RL, Huttly AK, Toscano-Underwood C, Feeney K, Welham S, Gooding MJ, Mills C, Edwards KJ, Shewry PR, Mitchell RA. Transcriptome analysis of grain development in hexaploid wheat. BMC Genomics 2008, 9:121. 10.1186/1471-2164-9-121, 2292175, 18325108.
47. Jiao Y, Song W, Zhang M, Lai J. Identification of novel maize miRNAs by measuring the precision of precursor processing. BMC Plant Biol 2011, 11:141. 10.1186/1471-2229-11-141, 3214924, 22014170.
48. Zhang L, Chia JM, Kumari S, Stein JC, Liu Z, Narechania A, Maher CA, Guill K, McMullen MD, Ware D. A genome-wide characterization of microRNA genes in maize. PLoS Genet 2009, 5(11):e1000716. 10.1371/journal.pgen.1000716, 2773440, 19936050.
49. Kang M, Zhao Q, Zhu D, Yu J. Characterization of microRNAs expression during maize seed development. BMC Genomics 2012, 13:360. 10.1186/1471-2164-13-360, 3468377, 22853295.
50. Lan Y, Su N, Shen Y, Zhang R, Wu F, Cheng Z, Wang J, Zhang X, Guo X, Lei C, Jiang L, Mao L, Wan J. Identification of novel MiRNAs and MiRNA expression profiling during grain development in indica rice. BMC Genomics 2012, 13:264. 10.1186/1471-2164-13-264, 3505464, 22721355.
51. Heisel SE, Zhang Y, Allen E, Guo L, Reynolds TL, Yang X, Kovalic D, Roberts JK. Characterization of unique small RNA populations from rice grain. PLoS One 2008, 3(8):e2871. 10.1371/journal.pone.0002871, 2518513, 18716673.
52. Wu L, Zhou H, Zhang Q, Zhang J, Ni F, Liu C, Qi Y. DNA methylation mediated by a microRNA pathway. Mol Cell 2010, 38(3):465-475. 10.1016/j.molcel.2010.03.008, 20381393.
53. Kozomara A, Griffiths-Jones S. miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res 2011, 39(Database issue):D152-D157. 3013655, 21037258.
54. Zhang Z, Yu J, Li D, Liu F, Zhou X, Wang T, Ling Y, Su Z. PMRD: plant microRNA database. Nucleic Acids Res 2010, 38(Database issue):D806-D813. 2808885, 19808935.
55. Thimm O, Blasing O, Gibon Y, Nagel A, Meyer S, Kruger P, Selbig J, Muller LA, Rhee SY, Stitt M. MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J Cell Mol Biol 2004, 37(6):914-939.
56. DOIG RI, COLBORNE AJ, MORRIS G, LAIDMAN DL. The induction of glyoxysomal enzyme activities in the aleurone cells of germinating wheat. J Exp Bot 1975, 26(3):387-398.
57. Gubler F, Kalla R, Roberts JK, Jacobsen JV. Gibberellin-regulated expression of a myb gene in barley aleurone cells: evidence for Myb transactivation of a high-pI alpha-amylase gene promoter. Plant Cell 1995, 7(11):1879-1891. 161046, 8535141.
58. Cuperus JT, Fahlgren N, Carrington JC. Evolution and functional diversification of MIRNA genes. Plant Cell 2011, 23(2):431-442. 10.1105/tpc.110.082784, 3077775, 21317375.
59. Weijers D, Franke-van Dijk M, Vencken RJ, Quint A, Hooykaas P, Offringa R. An Arabidopsis minute-like phenotype caused by a semi-dominant mutation in a ribosomal protein S5 gene. Development 2001, 128(21):4289-4299.
60. Tzafrir I, Pena-Muralla R, Dickerman A, Berg M, Rogers R, Hutchens S, Sweeney TC, McElver J, Aux G, Patton D, Meinke D. Identification of genes required for embryo development in Arabidopsis. Plant Physiol 2004, 135(3):1206-1220. 10.1104/pp.104.045179, 519041, 15266054.
61. Byrne ME. A role for the ribosome in development. Trends Plant Sci 2009, 14(9):512-519. 10.1016/j.tplants.2009.06.009, 19716746.
62. Gill BS, Appels R, Botha-Oberholster AM, Buell CR, Bennetzen JL, Chalhoub B, Chumley F, Dvorak J, Iwanaga M, Keller B, Li W, McCombie WR, Ogihara Y, Quetier F, Sasaki T. A workshop report on wheat genome sequencing: international genome research on wheat consortium. Genetics 2004, 168(2):1087-1096. 10.1534/genetics.104.034769, 1448818, 15514080.
63. Xue LJ, Zhang JJ, Xue HW. Characterization and expression profiles of miRNAs in rice seeds. Nucleic Acids Res 2009, 37(3):916-930. 10.1093/nar/gkn998, 2647296, 19103661.
64. Curaba J, Spriggs A, Taylor J, Li Z, Helliwell C. miRNA regulation in the early development of barley seed. BMC Plant Biol 2012, 12:120. 10.1186/1471-2229-12-120, 3443071, 22838835.
65. Song QX, Liu YF, Hu XY, Zhang WK, Ma B, Chen SY, Zhang JS. Identification of miRNAs and their target genes in developing soybean seeds by deep sequencing. BMC Plant Biol 2011, 11:5. 10.1186/1471-2229-11-5, 3023735, 21219599.
66. Nodine MD, Bartel DP. MicroRNAs prevent precocious gene expression and enable pattern formation during plant embryogenesis. Genes Dev 2010, 24(23):2678-2692. 10.1101/gad.1986710, 2994041, 21123653.
67. Schwab R, Voinnet O. RNA silencing amplification in plants: size matters. Proc Natl Acad Sci U S A 2010, 107(34):14945-14946. 10.1073/pnas.1009416107, 2930571, 20709960.
68. Berrier A, Ulbricht R, Bonn M, Rivas JG. Ultrafast active control of localized surface plasmon resonances in silicon bowtie antennas. Opt Express 2010, 18(22):23226-23235. 10.1364/OE.18.023226, 21164664.
69. Meyers BC, Axtell MJ, Bartel B, Bartel DP, Baulcombe D, Bowman JL, Cao X, Carrington JC, Chen X, Green PJ, Griffiths-Jones S, Jacobsen SE, Mallory AC, Martienssen RA, Poethig RS, Qi Y, Vaucheret H, Voinnet O, Watanabe Y, Weigel D, Zhu JK. Criteria for annotation of plant MicroRNAs. Plant cell 2008, 20(12):3186-3190. 10.1105/tpc.108.064311, 2630443, 19074682.
70. Addo-Quaye C, Miller W, Axtell MJ. CleaveLand: a pipeline for using degradome data to find cleaved small RNA targets. Bioinformatics 2009, 25(1):130-131. 10.1093/bioinformatics/btn604, 3202307, 19017659.
71. Rice P, Longden I, Bleasby A. EMBOSS: the European molecular biology open software suite. Trends Gen TIG 2000, 16(6):276-277.